Research report
Object and food novelty induce distinct patterns of c-fos immunoreactivity in amygdala and striatum in domestic male chicks (Gallus gallus domesticus)

https://doi.org/10.1016/j.bbr.2019.112453Get rights and content

Highlights

  • The neural bases of neophobia in birds were investigated by immunohistochemistry.

  • C-fos expression in the amygdala depends on the type of novelty.

  • C-fos expression in the striatum is similar following object or food novelty.

  • The motivational and limbic systems are involved in neophobia in chicks.

Abstract

Avoidance of novelty, termed neophobia, protects animals from potential dangers but can also impair their adaptation to novel environments or food resources. This behaviour is particularly well described in birds but the neurobiological correlates remain unexplored. Here, we measured neuronal activity in the amygdala and the striatum, two brain regions believed to be involved in novelty detection, by labelling the early gene c-fos following chicks exposure to a novel food (NF), a novel object (NO) or a familiar food (FF). NF and NO chicks showed significantly longer latencies to touch the food, less time eating and emitted more fear-vocalizations than control chicks. Latency to touch the food was also longer for NO than for NF chicks. Significantly higher densities of c-fos positive cells were present in all the nuclei of the arcopallium/amygdala of NF and NO chicks compared to FF chicks. Also, NO chicks showed higher positive cell densities than NF chicks in the posterior amygdaloid, the intermediate and the medial arcopallium. Exposure to novel food or object induced a similar increase in c-fos expression in the nucleus accumbens and the medial striatum. Our data provide evidence activation of the arcopallium/amygdala is specific of the type of novelty. The activation of striatum may be more related to novelty seeking.

Introduction

A large range of avian species exhibit neophobia, a reluctance to approach novelty. This behaviour brings about both positive and negative consequences on their survival. It allows animals to adapt their reactions to changes or potential threats in their environment [1]. When strongly expressed, neophobia can also impair foraging flexibility, innovations, and reduce home range size or species’ niche breadth [[1], [2], [3], [4], [5]]. On farm, it can be a cause for concern in relation to bird welfare as it can impair the capacity of fowl to adapt to changes in their feeding regime [6]. Neophobia is also considered a trait to estimate behavioural syndromes or copying styles within populations, that is to say birds’ capacity to cope behaviourally and physiologically with stressful environmental challenges [3,4,[7], [8], [9]].

Although response to novelty has been shown to be important for bird’s adaptation and survival, few studies investigated its neuro-physiological bases. Japanese quail (Coturnix coturnix japonica) exposed repeatedly to the sudden introduction of a novel object in their home cage showed a significant rise in plasma corticosterone levels [13]. This endocrine response induced by a novel object was also found in great tits (Parus major) exposed to a novel perch in their home cage [14]. These results indicate exposure to novelty induces fear-related responses in birds that are likely underpinned by the activation of brain regions involved in fear or emotions. In line with this, previous studies demonstrated that rats with amygdala lesions, a brain region involved in the processing of emotional cues and fear leaning, show attenuated response to novelty [[10], [11], [12], [13]]. In birds, wild black-capped chickadees from Alaska that showed less of a neophobic response to a novel object than their Kansas counterpart [14], had a larger arcopallium volume, a brain region that some authors considered as the homolog of the mammalian amygdala [15]. This study highlighted that the birds from Alaska had a higher density of neurons in the lateral striatum, believed to be the homolog of the mammalian caudate nucleus and putamen. The mammalian striatum has been repeatedly shown to be involved in novelty seeking, motivation and reward processing [[16], [17], [18], [19], [20]]. These findings indicate that neophobia in birds is not only a fear response but also related to the processing of motivation triggering cues and goal directed behaviours. However, a clear relationship between neophobia and amygdala/arcopallium or striatum subnuclei activation still need to be investigated in birds.

To better characterize the neural circuit activated by novelty in birds, we labelled chicks brain with the early gene c-fos following exposure to novel food and novel object. In birds and mammals, c-fos cellular expression is widely used to reliably map the brain activity underlying behaviours such as fear-related behaviours, decision-making or learning [[21], [22], [23]]. This study was conducted in the domestic chicken (Gallus gallus domesticus) which is particularly appropriate for such a study. Food and object neophobia are easily observed in young chicks in experimental conditions. A brain atlas as well as immunohistochemical procedures for studying c-fos expression are well established [[24], [25], [26], [27]]. We studied c-fos expression following exposure to both novel food and object because both types of neophobia have been described in chicks and can have an impact on animal adaptation. Moreover, we previously observed that responses to novel food did not correlate with responses to a novel object and were milder [28]. This may suggest both types of neophobia may be associated with specific and distinct brain activations. We investigated c-fos expression in different subnuclei of both the arcopallium/amygdala and striatum, as these brain structures has previously been found to be engaged in novelty detection [11,15].

Section snippets

Ethics statement

All birds were maintained at the Experimental Unit PEAT of INRA (Nouzilly, France, license number B-37-175-1). All experiments were approved by the Ethics Committee for Animal Experimentation of Val de Loire, CEEA Vdl (reference number 2012-10-6) and were performed in accordance with the European Communities Council Directive 2010/63/UE. The remaining chicks were sold at the end of the experiment.

Chicks and housing conditions

The layer breeder Novogen (SCEA JEGOU, France) provided eggs from White Leghorn layers. The eggs

Behavioural characterization

We found a significant effect of the treatment on the latency to touch the food (F2,20 = 32.6, P <  0.01; Fig. 3). Post-hoc analyses showed that NF and NO chicks had longer latencies to touch the food than control FF chicks (P <  0.01 for both comparisons) and, that NO chicks had longer latencies than NF chicks (P =  0.05; Fig. 3). The time spent eating during testing differed significantly between treatments (F2,20 = 24.02, P <  0.01; Fig. 3). Post-hoc analyses showed that the time spent

Discussion

Our aim was to deepen our understanding of the underlying mechanisms of neophobia in birds. Clear behavioral differences were observed when chicks are exposed to novel food or object compared to the control condition. Chicks exposed to either novel food or object showed higher latencies to touch the food, lower time spent eating and a higher number of fear-trill vocalizations compared to controls. In addition, NO chicks showed a higher latency to touch food than NF chicks. At the brain level,

CRediT authorship contribution statement

Emilie C. Perez: Conceptualization, Methodology, Formal analysis, Investigation, Writing - original draft, Visualization. Maryse Meurisse: Methodology, Investigation, Resources, Supervision. Lucile Hervé: Investigation. Marion Georgelin: Methodology, Formal analysis, Investigation. Paul Constantin: Investigation. Fabien Cornilleau: Investigation. Scott A. Love: Writing - review & editing. Frédéric Lévy: Writing - review & editing. Ludovic Calandreau: Conceptualization, Methodology, Formal

Declaration of Competing Interest

None.

Acknowledgments

All birds were maintained at the PEAT experimental unit, INRA, Nouzilly, France. We are grateful to all members of the unit for taking care of the chicks. This work has benefited from the facilities and expertise of the "Plateforme d'imagerie Cellulaire" (PIC) of the UMR-PRC. We are grateful to T. Burlot (Novogen, France) who freely provided all the eggs. This work was supported by the French National Research Agency (ANR); project FeedPhobic ANR-12-JSV7-0011-01. The funding agency had no

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